Abstract: Necropsy of 2 4-year-old southern crowned pigeons (Goura
scheepmakeri) that died from a presumed case of botulism revealed
hundreds of small, cyst-like structures in the pectoral subcutaneous
tissues. The structures were identified as heteromorphic deutonymphs of
Hypodectes propus (Order Astigmata) of the family Hypoderatidae. The
immobile, immature hypopi were individually encapsulated, mostly in
adipose tissue, and evoked only a mild inflammatory infiltration of
predominately macrophages with some heterophilic granulocytes. The
infection was not considered a serious health problem and was
interpreted as an incidental finding. To our knowledge, this is a new
host record for H propus.

A pair of 4-year-old southern crowned pigeons (Goura scheepmakeri)
kept at the Copenhagen Zoo in Denmark died from a presumed case of
botulism. Both birds were born in captivity. The male was hatched and
raised at the Copenhagen Zoo, whereas the female was hatched in the Hong
Kong Zoological and Botanical Gardens and was imported to Denmark via
the Rotterdam Zoo approximately 6 months before its death. The pair were
brooding their first egg when they died; the likely source of toxins was
contaminated feed. In both cases, the birds were lethargic and
demonstrated paralysis of the neck and partial paralysis of the wings.
Supportive treatment with fluids, nonsteriodal anti-inflammatory drugs,
and antibiotics was unsuccessful, and the birds died the next day after
exhibiting clinical signs.

At necropsy, the carcasses of both pigeons appeared grossly normal.
White, ovoid-cylindrical, cyst-like structures approximately 1 mm long
were found in the subcutaneous adipose tissue covering the pectoral
musculature and extending caudally along the sides of the body (Fig 1a).
The female bird displayed hundreds of these structures, whereas the male
had substantially more. On microscopic examination, the structures were
classified as sack-like mites. The skin covering the affected areas
appeared slightly swollen. The underlying subcutaneous connective tissue
was swollen and hyperemic. No other significant macroscopic findings
were found. Selected tissue samples of heart, lungs, liver, spleen,
kidneys, gastrointestinal tract, and brain were collected in 10%
formalin and processed routinely for histopathologic examination. Mites
were collected and stored in 70% ethanol, and a subsample of mites was
prepared for electron microscopy (Fig 2). Mites were subsequently
mounted in Hoyer's media under Glyptal epoxy enamel--ringed
OO-thickness cover glasses. They were identified as heteromorphic
deutonymphs (hypopi) of Hypodectes propus (Nitzch, 1861). (1,2)

Microscopically, cross-sections of hypoderatid deutonymphs were
present in the subcutaneous pectoral tissues throughout the affected
areas (Fig lb). Mites were present predominantly in the subcutaneous
adipose layer, but some were found in the dermis and underlying
musculature. The cross-sectioned hypopi were individually encapsulated
and had no contact with each other. Surrounding the deutonymphs were
varying numbers of primarily macrophages and fewer heterophilic
granulocytes. This inflammatory response was most pronounced in the more
heavily infected male individual. Histopathologic abnormalities were not
detected in any of the other sampled tissues.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Discussion

Due to their small size, astigmatic mites (Subclass Acari) are able
to survive in habitats and ecological niches unavailable to larger
arthropods, including a multitude of microhabitats on and in the bodies
of the host animals. (3) Hypodectes propus is generally associated with
pigeons, herons, and egrets. (3-6) This species has developed a complex
symbiotic relationship with its hosts by exploiting resources of their
subcutaneous adipose tissues? (1-3) During their sojourn within the
host, the hypopi increase 10-fold in size (4,5) and become widely
dispersed as a result of the migratory behavior of their hosts. (4,7)
This phoretic relationship compensates for the disadvantages of small
size in longdistance migration and the lack of morphologic adaptation
(eg, wings) for independent migration. (6) To our knowledge, this is the
first description of hypopi of H propus in the southern crowned pigeon
(Order Columbiformes).

The deutonymph or hypopus is a developmental instar of mites, and
in H propus it is one of 5 juvenile stages including the prelarva,
larva, protonymph, deutonymph, and tritonymph. (5) The deutonymph
differs from the other stages by the absence of functional mouthparts
and an alimentary tract. (4) However, this stage is the only fully
parasitic stage (5) and this stage obtains all the nutrition for the
entire life cycle of the parasite (3,4) through its exoskeleton. (6,8)
Deutonymphs penetrate the skin of their hosts a few days after young
birds hatch in the nest. (1,3) The mechanism by which they enter the
skin is still unknown. The hypopi persist and grow in the subcutaneous
adipose tissue until the host reaches maturity and begins to incubate
its eggs. (4) All other life stages are residents in the nests of their
hosts. (4,9) It is considered that the development and exodus of the
mature deutonymph from the host depends on the hormone prolactin in the
host during brooding. (4) The inflammatory response to hypoderatid mites
in the adipose and other subcutaneous tissues of various birds ranges
from a few foamy macrophages and plasma cells in the vicinity of the
living hypopi in some hosts to a severe and diffuse granulomatous
inflammation in some heavily infected birds. (10) Dead and degenerating
hypopi may be attended by a more organized fibroplasia with a
surrounding cuff of Langhans' giant cells and masses of epithelioid
histiocytes, lymphocytes, plasma cells, and eosinophils. (10) However,
most studies indicate that hypopi have little effect on the health of
the host and are usually regarded as incidental findings at necropsy.
(9,10) In accordance with these studies, infection with H propus did not
appear to be the cause of death of the crowned pigeons in this case.

Considering the behavior and life cycle of H propus, these southern
crowned pigeons were most likely infected as chicks in their original
environments. However, it is notable that none of the zoological gardens
involved with this pair have previously seen cases of acariasis caused
by H propus in any bird species. The exact source of infection is
therefore unknown. Hypopi are resting deutonymphs and because they are
hormonally activated, presumably may exist in a bird for long periods.
This would explain their persistence for 3 years in the birds that had
not previously nested.

Acknowledgments: We acknowledge the assistance of the late Mr Jose
Bresciani of the University of Copenhagen for producing the electron
microscopic images. We also thank Mr Rob Belterman of Rotterdam Zoo and
Mr Leonard Ting of Hong Kong SAR Government.